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Perspective

Frontiers in Virology ·

Volume 6 - 2026 | https://doi.org/10.3389/fviro.2026.1897263

An eco-evolutionary perspective on endemic persistence and invasive emergence of begomoviruses in Mexico

  • Katia Aviña-Padilla1
  • Flor C. Alcántar-Aguirre2
  • Erika J. Zamora-Macorra3
  • Ubilfrido Vasquez-Gutierrez4
  • Jimena Carrillo-Tripp5
  • Alfredo Diaz-Lara6*corresponding author
  1. 1Department of Cell Biology, Centro de Investigación y de Estudios Avanzados del Instituto Politecnico Nacional, Mexico, Mexico
  2. 2Department of Developmental Neurobiology and Neurophysiology, Institute of Neurobiology, Universidad Nacional Autónoma de Mexico, Queretaro, Mexico
  3. 3Department of Agricultural Preparatory School, Universidad Autónoma Chapingo, Estado de Mexico, Mexico, Mexico
  4. 4Department of Parasitology, Universidad Autonoma Agraria Antonio Narro, Saltillo, Mexico
  5. 5Department of Microbiology, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Baja California, Mexico
  6. 6School of Engineering and Sciences, Tecnologico de Monterrey, Queretaro, Mexico
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Abstract

Here we present a conceptual eco-evolutionary perspective on begomovirus emergence, motivated by the observation that these globally important plant DNA viruses of tropical and subtropical agriculture are frequently interpreted through isolated, pathogen-centered case studies. We propose a broader framework in which begomoviruses in agroecosystems operate under two contrasting but interconnected regimes: i) endemic persistence, and ii) invasive emergence. Endemic regimes are characterized by ecological continuity, recurrent mixed infections, local recombination, and long-term circulation within regional host–vector networks. Invasive regimes are characterized by biological introduction, rapid spatial expansion, strong anthropogenic selection, and post-introduction adaptation. Using Mexican begomovirus systems as a conceptual model, we contrast pepper huasteco yellow vein virus (PHYVV, Begomovirus capsicumhuastecoense) and pepper golden mosaic virus (PepGMV, B. capsicummusivi), which illustrate endemic persistence in pepper-associated agroecosystems, with tomato yellow leaf curl virus (TYLCV, B. coheni), which exemplifies invasive emergence in intensive tomato production systems. Both regimes share mechanisms such as whitefly (Bemisia tabaci)-mediated transmission, mixed infection, and recombination, but they differ in evolutionary tempo, spatial scale, and ecological context. Recognizing endemic and invasive regimes as part of a continuum may improve surveillance, risk assessment, and anticipatory management of begomovirus diseases.

Keywords

1 Introduction

Begomoviruses, members of the genus Begomovirus in the family Geminiviridae, represent one of the most significant viral threats to agriculture in tropical and subtropical regions, where their emergence and persistence are tightly linked to ecological complexity and agricultural intensification (1, 2). Their epidemiological dynamics are not determined solely by virus–host interactions, but rather by a multiscale network involving susceptible crops, alternative plant reservoirs, insect vectors, viral genetic diversity, environmental pressures, and human-driven agricultural practices (3). In this context, begomovirus epidemics should not be interpreted as isolated phytopathological events, but instead as dynamic eco-evolutionary processes shaped by ecological connectivity and adaptive interactions across agroecosystems (4). Here, we propose a conceptual perspective in which begomoviruses can be understood through two interconnected eco-evolutionary regimes, (i) endemic persistence and (ii) invasive emergence. Endemic persistence refers to viral systems that remain regionally established over long temporal scales, coexisting with local crops, weeds, and vector populations under relatively stable ecological interactions. In contrast, invasive emergence involves the introduction and rapid expansion of viral lineages into novel agroecological contexts, frequently associated with shifts in vector populations, crop intensification, trade-mediated dispersal, and ecological disturbance (5). Importantly, these regimes are not mutually exclusive; rather, they coexist and interact within shared agricultural landscapes, creating opportunities for mixed infections, recombination, host shifts, and the generation of novel epidemiological trajectories.

To operationalize the endemic–invasive continuum, we propose characterizing viral regimes along four empirically measurable axes: (i) temporal persistence, measured as years of documented regional circulation; (ii) geographic range breadth, measured as the number of distinct production regions with confirmed detection; (iii) mixed-infection frequency, measured as the proportion of field-collected samples co-infected by two or more begomovirus species; and (iv) recombination incidence, estimated from the frequency of recombination events detected per genomic dataset in published surveys. Under this framework, the pepper huasteco yellow vein virus (PHYVV, Begomovirus capsicumhuastecoense) and pepper golden mosaic virus (PepGMV B. capsicummusivi), pathosystems rank high on axes (i)–(iii), consistent with long-term endemic persistence, whereas tomato yellow leaf curl virus (TYLCV, B. coheni), ranks high on axis (ii), reflecting its rapid geographic expansion, but lower on axes (i) and (iii) within Mexican systems, consistent with its recent introduction. Position along these axes is dynamic and may shift as ecological and epidemiological conditions change, reinforcing the continuum rather than categorical nature of these regimes. A formally weighted index is beyond the scope of this perspective; in future work, however, these axes could be normalized (e.g., to a 0–1 scale per axis) and combined into a composite continuum-position score that would serve as a quantitative proxy for locating each pathosystem along the endemic–invasive gradient and for tracking directional shifts over time.

Mexico provides an especially relevant framework for exploring these processes because its pepper- and tomato-associated agroecosystems contain both regionally persistent begomoviruses and recently introduced invasive lineages, all within highly connected production systems dominated by whitefly-mediated transmission. We use PHYVV/PepGMV and TYLCV in Mexican agroecosystems as contrasting empirical models of these two regimes. We argue that the interaction between endemic and invasive viral regimes may generate critical surveillance-relevant contact zones where ecological overlap increases the probability of coinfection, recombination, and adaptive innovation. We define surveillance-relevant contact zones as agroecological areas where endemic and invasive begomovirus regimes spatially or temporally co-occur within shared host and vector networks, thereby creating conditions that elevate the probability of mixed infection, genomic exchange, and the emergence of novel viral variants. Such zones may function as evolutionary interfaces that facilitate the emergence of novel viral variants with altered host range, transmission efficiency, or pathogenicity. From this perspective, begomovirus epidemiology should be examined not only through disease incidence, but also through the ecological and evolutionary processes that govern viral persistence, invasion, and diversification across interconnected agroecosystems. The conceptual framework integrating endemic persistence, invasive emergence, mixed infections, recombination potential, and epidemiological transition zones is summarized in Figure 1.

Ecological and evolutionary dynamics of endemic and invasive begomoviruses across Mexican agroecosystems. **(A)** Endemic persistence is characterized by locally connected agroecosystems in which native begomoviruses circulate between wild and cultivated pepper hosts through low-intensity transmission mediated by *B. tabaci*. These endemic viral communities exhibit ecological stability, gradual diversification, and recombination within relatively balanced host–vector networks. **(B)** The contact zone represents the ecological and evolutionary interface where endemic and invasive viromes interact through shared vectors, co-infection events, and overlapping host ranges, with bidirectional spillover of viral lineages between cultivated and non-cultivated hosts (endemic and invasive regimes each acting as both source and recipient). **(C)** Invasive emergence illustrates the introduction of TYLCV-like viruses into intensified tomato production systems, where high vector pressure, dense monocultures, and strong epidemiological connectivity promote rapid epidemic spread, host shifts, and accelerated viral adaptation. These interactions may facilitate viral recombination, genetic exchange, and the emergence of novel recombinant begomoviruses with expanded adaptive potential. Together, the figure highlights how agroecosystem interfaces can shape viral diversification and evolutionary innovation in plant virus pathosystems. Source: Created using [BioRender.com](https://www.BioRender.com).
Figure 1. Ecological and evolutionary dynamics of endemic and invasive begomoviruses across Mexican agroecosystems. (A) Endemic persistence is characterized by locally connected agroecosystems in which native begomoviruses circulate between wild and cultivated pepper hosts through low-intensity transmission mediated by B. tabaci. These endemic viral communities exhibit ecological stability, gradual diversification, and recombination within relatively balanced host–vector networks. (B) The contact zone represents the ecological and evolutionary interface where endemic and invasive viromes interact through shared vectors, co-infection events, and overlapping host ranges, with bidirectional spillover of viral lineages between cultivated and non-cultivated hosts (endemic and invasive regimes each acting as both source and recipient). (C) Invasive emergence illustrates the introduction of TYLCV-like viruses into intensified tomato production systems, where high vector pressure, dense monocultures, and strong epidemiological connectivity promote rapid epidemic spread, host shifts, and accelerated viral adaptation. These interactions may facilitate viral recombination, genetic exchange, and the emergence of novel recombinant begomoviruses with expanded adaptive potential. Together, the figure highlights how agroecosystem interfaces can shape viral diversification and evolutionary innovation in plant virus pathosystems. Source: Created using BioRender.com.

Unlike previous reviews on begomovirus ecology and emergence, which have addressed recombination, vector biology, or geographic spread as largely independent phenomena, the present perspective contributes in two explicit ways. First, it integrates endemic persistence and invasive emergence within a unified eco-evolutionary continuum framework, rather than treating them as separate epidemiological categories. Second, it centers the Mexican agroecosystem with PHYVV/PepGMV and TYLCV as contrasting yet interacting case studies, as the primary empirical reference system for eco-evolutionary surveillance design. This Mexico-centered approach is justified by the exceptional diversity of documented begomovirus–host–vector interactions in Mexican agroecosystems, and it provides a translatable conceptual template applicable to other regions characterized by comparable biological and epidemiological complexity. To establish this framework, it is first necessary to examine the biological attributes of begomoviruses and the ecological processes that shape their evolutionary dynamics.

2 Begomovirus biology and eco-evolutionary context

Begomoviruses are plant-infecting single-stranded DNA viruses transmitted by the whitefly (Bemisia tabaci) (1, 6). Members of the genus Begomovirus mainly infect dicotyledonous plants and display either monopartite or bipartite genome organization. Their compact genomes encode functions required for replication, movement, encapsidation, and vector-mediated transmission, while also enabling rapid diversification through mutation, recombination, and genomic component exchange (7–9). Recombination is a major evolutionary process shaping begomovirus diversification. Comparative analyses of DNA-A and DNA-A-like components have identified recombination hot- and cold-spots, suggesting that genomic exchange is constrained by functional and structural organization rather than occurring randomly (10). Phylogeographic analyses of coat protein and replication-associated protein sequences further reveal strong geographic structure among begomovirus populations, indicating that regional ecological conditions and dispersal histories contribute to diversification patterns (11). Their epidemiology is also strongly influenced by host–vector connectivity. Bemisia tabaci is now recognized as a complex of cryptic lineages differing in geographic distribution, host range, transmission efficiency, and invasion potential (12). Through its vector activity, the whitefly interconnects cultivated crops, weeds, ruderal vegetation, and alternative hosts within broader epidemiological networks, facilitating begomovirus circulation across agricultural landscapes (13).

Mixed infection constitutes another important component of their biology. Experimental studies have demonstrated synergistic interactions between PHYVV/PepGMV in pepper (Capsicum annuum) plants, resulting in increased symptom severity and viral DNA accumulation (14). Superinfection by PHYVV can additionally modify recovery responses in PepGMV-infected plants through changes in viral DNA accumulation, DNA methylation, and viral chromatin state (15). More recent studies indicate that coinfection and recombination may generate recombinant variants with altered competitive capacity and epidemiological behavior, reinforcing the importance of ecological contact zones where endemic and invasive viral lineages overlap (16, 17).

Previous studies have shown that whitefly-transmitted geminiviruses in Latin America have emerged and disseminated in association with susceptible crops, agricultural intensification, and transmission by the whitefly complex (4). At the same time, comparative analyses of begomovirus evolution demonstrate that recombination is influenced by genomic constraints and may contribute to host shifts, diversification, and viral emergence (10, 18). Together, these observations support the interpretation of begomovirus epidemiology as a dynamic interaction between ecological connectivity and evolutionary processes operating across agricultural landscapes. Within this eco-evolutionary framework, endemic systems provide an opportunity to examine how long-term virus–host–vector interactions maintain viral diversity and ecological stability before transitions toward invasive dynamics occur. The Mexican PHYVV/PepGMV pathosystem represents one of the best-characterized examples of this endemic condition.

2.1 Endemic persistence in Mexican begomovirus systems: the PHYVV/PepGMV model

Endemic begomovirus systems should not be interpreted as static viral reservoirs, but rather as dynamic ecological networks in which host availability, whitefly-mediated transmission, mixed infections, and genetic exchange collectively contribute to long-term viral persistence. In Mexican pepper-associated agroecosystems, PHYVV and PepGMV represent a useful model for understanding endemic persistence under conditions of sustained ecological connectivity and recurrent viral interaction. PHYVV was originally molecularly characterized from northern Mexico as a bipartite begomovirus (19). PepGMV was similarly described as a bipartite begomovirus infecting pepper plants in Mexico (20). Both viruses share a broad host range within solanaceous crops and have been frequently co-detected in production regions of northern and central Mexico, suggesting overlapping ecological niches. Subsequent field surveys in the state of Sinaloa revealed high prevalence of both PHYVV and PepGMV in symptomatic chili pepper plants, with PHYVV detected in 74.4% and PepGMV in 53.7% of analyzed samples, including frequent PHYVV/PepGMV mixed infections (21). These observations suggest that both viruses circulate within overlapping epidemiological niches rather than as isolated pathogenic entities.

Experimental transmission assays demonstrated that the whitefly can efficiently acquire and transmit PHYVV and PepGMV individually or simultaneously to chili pepper plants (22). This capacity for co-transmission may create ecological conditions that facilitate coinfection and increase opportunities for viral interaction within shared hosts. Consistent with this, experimental studies have shown that PHYVV and PepGMV interact synergistically during mixed infection, leading to increased symptom severity and elevated viral DNA accumulation (14).

Evidence from Mexican chiltepin pepper-associated systems further supports the eco-evolutionary relevance of these interactions. Rodelo-Urrego et al. (23) showed that ecosystem biodiversity modulates PHYVV and PepGMV genetic diversity in a virus-specific manner, while also detecting recombinant and reassortant viral variants. From this perspective, the PHYVV/PepGMV pathosystem can be cautiously interpreted as an endemic recombination arena in which long-term ecological coexistence, bipartite genome organization, mixed infections, and persistent vector circulation may collectively create conditions favorable for diversification and evolutionary experimentation. Importantly, this interpretation does not imply that recombination alone explains begomovirus diversity, but rather that endemic agroecosystems may function as stable evolutionary interfaces where ecological persistence continuously generates opportunities for genetic innovation.

Taken together, the evidence reviewed above positions the PHYVV/PepGMV pathosystem toward the endemic pole of the eco-evolutionary continuum. The combination of long-term regional persistence, efficient co-transmission by the whitefly, synergistic mixed-infection interactions, and documented recombination and reassortment collectively characterizes an endemic regime in which ecological continuity drives evolutionary opportunity. Critically, this regime does not represent stasis: the recurrent generation of recombinant and reassortant variants means that endemic systems are evolutionarily active arenas, not inert reservoirs. This distinction—between ecological stability and evolutionary stasis—is central to understanding why endemic begomoviruses may, under altered ecological conditions, shift position along the continuum toward emergence.

A critical question for the continuum model is why PHYVV and PepGMV have not transitioned to an invasive regime in other regions. Several non-mutually exclusive factors likely contribute. First, both viruses display strong geographic structuring consistent with regional adaptation: their phylogenetic diversity is largely concentrated within Mexican solanaceous agroecosystems, suggesting that long-term coevolution with local host genotypes and the whitefly lineages has produced fitness optima that may not be competitive outside this ecological context. Second, unlike TYLCV, which benefits from global trade in tomato seedlings and planting material as a dispersal pathway, PHYVV and PepGMV are primarily associated with pepper cultivation systems that have fewer international trade-mediated dissemination routes. Third, the bipartite genome organization of PHYVV and PepGMV imposes a co-dispersal requirement for both DNA-A and DNA-B components, potentially constraining long-distance spread relative to monopartite viruses such as TYLCV. These constraints collectively position PHYVV and PepGMV toward the endemic pole of the continuum and illustrate how biological and agroecological factors interact to determine regime stability. The opposite end of this continuum is represented by introduced viruses that successfully overcome ecological and dispersal barriers, establishing persistent transmission networks in new environments. TYLCV exemplifies this alternative evolutionary trajectory and provides a complementary model for understanding the mechanisms underlying invasive emergence following introduction.

2.2 Invasive emergence and post-introduction adaptation: the TYLCV model

Introduced begomoviruses represent a contrasting eco-evolutionary regime characterized by rapid establishment, geographic expansion, and adaptation within already occupied epidemiological landscapes. TYLCV is one of the most globally disseminated begomoviruses and is associated with tomato yellow leaf curl disease (TYLCD), a viral disease complex with major impacts on tomato (Solanum lycopersicum) production worldwide (24). Phylogeographic analyses suggest a probable Middle Eastern origin for TYLCV followed by extensive global dissemination driven by agricultural trade, vector expansion, and intensive crop production systems (5).

In Mexico, TYLCV was initially detected in symptomatic tomato plants from the Yucatán Peninsula and was subsequently reported in Sinaloa during the 2005–2006 tomato-growing seasons (25, 26). Viral sequences from these outbreaks displayed high nucleotide identity with TYLCV isolates previously described from the Caribbean region and Florida, supporting the interpretation of recent introduction events linked to transregional viral movement. Unlike endemic begomovirus systems shaped by long-term ecological coexistence, TYLCV emergence in Mexico reflects the arrival of an invasive viral lineage into agroecosystems already containing resident begomovirus communities.

The successful establishment of TYLCV following introduction is likely favored by multiple ecological and agricultural factors, including intensive tomato production, continuous availability of susceptible hosts, and efficient vector-mediated transmission by the Bemisia tabaci cryptic species complex, a group of morphologically similar but genetically distinct whitefly lineages with differing transmission efficiencies and invasion capacities (12, 13). Modern production systems may additionally generate strong anthropogenic selection pressures through crop management practices, insecticide use, resistant cultivar deployment, and continuous cropping cycles. In Mexico, begomovirus control in tomato production systems is further influenced by diagnostic capacity, vector pressure, and integrated disease management strategies (27a).

Following establishment, TYLCV populations may undergo additional adaptive processes associated with host resistance and management-driven selection. In Mediterranean TYLCD systems, the deployment of resistant tomato cultivars has been associated with shifts in begomovirus population structure and viral composition (28). Similarly, recent analyses of the tomato ty-5 resistance network suggest that host resistance mechanisms can shape TYLCV–host interactions at both molecular and epidemiological levels (29). These observations support the idea that invasive begomovirus populations continue evolving after introduction through ongoing ecological and selective interactions within agricultural environments. In the Mexican context, García-Estrada et al. (27) reviewed virus management in tomato production systems in Sinaloa and Sonora and identified intensive insecticide use targeting the whitefly, continuous cropping schedules, and the incremental adoption of Ty-gene-carrying tomato hybrids as key drivers shaping viral epidemiology. Although studies directly quantifying TYLCV population shifts in response to resistant cultivar deployment in Mexico remain limited compared to the Mediterranean literature, the growing adoption of Ty-1, Ty-3, and ty-5 resistance genes in commercial hybrids across northern Mexican production regions constitutes a parallel selection context that warrants targeted molecular surveillance. Importantly, the consequences of TYLCV emergence also depend on its ecological overlap with resident begomovirus communities. In northern Mexico, TYLCV has been identified in double and triple infections involving PHYVV and/or PepGMV within pepper-associated disease complexes (30). Similar mixed infections in TYLCD systems outside Mexico have been associated with recombination events and the generation of novel begomovirus variants (18, 31, 32). Recent studies examining begomovirus coexistence, recombination dynamics, and satellite DNA interactions in tomato-associated systems further reinforce the view that tomato viral diseases should be interpreted as complex ecological assemblages rather than single-pathogen problems (33). From this perspective, interactions between TYLCV and resident Mexican begomoviruses should not be viewed as uniformly resulting in recombination or displacement, but rather as eco-evolutionary opportunities for diversification whose outcomes depend on local ecological context, vector dynamics, host composition, and patterns of viral coexistence.

These observations collectively position TYLCV toward the invasive pole of the continuum. Unlike PHYVV/PepGMV, whose persistence is maintained by deep ecological embedding within local host–vector networks, TYLCV’s establishment is driven by anthropogenic connectivity, rapid geographic expansion, and ongoing post-introduction adaptation. However, as TYLCV encounters resident Mexican begomoviruses in shared host and vector contexts, its evolutionary trajectory may increasingly incorporate features of endemic dynamics—mixed infections, local recombination, and host-range adjustment. This transition illustrates why the endemic–invasive distinction is better understood as a continuum than as a fixed categorical boundary.

2.3 Connections between endemic and invasive pathosystems

Rather than representing mutually exclusive categories, endemic and invasive pathosystems may coexist and interact within the same agroecosystem. In Mexico, TYLCV has been detected in association with PHYVV and/or PepGMV in pepper production systems of northern Mexico, demonstrating that resident and introduced begomoviruses can occupy overlapping ecological and epidemiological niches (30). Such coexistence exposes viruses with contrasting evolutionary histories to the same host species, vector populations, surrounding vegetation, and agricultural practices, creating evolutionary interfaces that connect the endemic and invasive ends of the continuum. These interfaces provide opportunities for ecological and evolutionary processes that are largely absent when each virus is considered independently. Mixed infections may modify transmission dynamics through interactions within shared hosts and vectors, while coinfection creates the potential for genomic exchange through recombination, one of the principal drivers of begomovirus diversification. Continued circulation within local agroecosystems may also promote host-range adjustment and regional adaptation of invasive viruses. Importantly, the presence of these ecological conditions should not be interpreted as evidence that recombination or displacement necessarily occurs in every system. Instead, they define environments in which such evolutionary processes become biologically plausible and therefore warrant surveillance.

The importance of these ecological interfaces is supported by high-throughput sequencing studies documenting the co-circulation of multiple begomovirus species and related genomic sequences in non-cultivated plants from northern-Pacific Mexico (34). These alternative hosts likely contribute to viral persistence, circulation, and connectivity beyond cultivated crops, increasing opportunities for interactions among endemic and invasive viruses. Similar ecological settings have been associated elsewhere with recombination and resistance-driven diversification in TYLCD pathosystems (28, 31, 32), although direct extrapolation to Mexican systems remains premature.

Together, these observations reinforce that invasion is not a terminal evolutionary state. As invasive viruses become embedded within resident ecological networks, they may progressively acquire characteristics associated with endemic persistence, whereas endemic viruses may themselves experience altered evolutionary trajectories following the arrival of invasive competitors. Consequently, the transition between endemicity and invasiveness should be viewed as a dynamic evolutionary process rather than a fixed categorical boundary, with ecological interfaces representing key locations for surveillance and early detection of evolutionary change.

3 Surveillance gaps and comparative insights

Current begomovirus surveillance strategies remain largely focused on symptomatic crop outbreaks and single-pathogen diagnostics, despite increasing evidence that begomovirus emergence is driven by broader ecological and evolutionary interactions involving vectors, weeds, intercrops, alternative hosts, agricultural intensification, and viral coexistence. If emergence is understood as a continuum shaped by these interacting processes, surveillance must also evolve from a reactive framework toward an eco-evolutionary approach that integrates genomic, ecological, and landscape-level information capable of identifying the interfaces where endemic and invasive viral systems converge and diversify.

For endemic systems such as PHYVV/PepGMV, future research should prioritize understanding how resident viral communities are maintained through long-term ecological connectivity involving alternative hosts, whitefly movement, mixed infections, and recombination potential (10, 20, 21, 23). In these systems, persistence is not solely determined by crop infection cycles but also by the existence of broader viral reservoirs distributed across surrounding vegetation and agroecological interfaces. This interpretation is supported by HTS analyses conducted in northern-Pacific Mexico, where Rodríguez-Negrete et al. (34) identified extensive begomovirus diversity in non-cultivated plants collected at crop–wild vegetation interfaces. Their study revealed begomovirus-associated DNA signatures in more than 60% of the sampled plants across multiple regions of Mexico, supporting the idea that non-cultivated vegetation may function as a regional reservoir and evolutionary interface for begomovirus maintenance and diversification.

Additional evidence from Mexico reinforces the ecological importance of weeds and alternative hosts in begomovirus epidemiology. García-Rodríguez et al. (35) identified a novel recombinant begomovirus, sida chlorotic leaf virus (SiChLV; B. sidaflavusfolii), in weeds belonging to the genera Sida and Malvastrum, while also detecting crop-associated begomoviruses infecting non-cultivated plants in Colima. The authors proposed that weeds may function simultaneously as reservoirs, incubators of viral diversity, and environments favoring recombination events capable of generating new viral variants. Importantly, these observations support the interpretation that endemic begomovirus systems in Mexico operate within interconnected ecological mosaics rather than isolated agricultural compartments.

For introduced systems such as TYLCV, surveillance priorities differ because the main epidemiological challenge involves early detection, monitoring of whitefly populations, and identification of overlap with resident begomovirus communities. As described before (30), TYLCV co-occurs with PHYVV and/or PepGMV in northern Mexico. Such findings suggest that introduced and endemic viruses may coexist within shared host and vector networks, creating surveillance-relevant contact zones where ecological overlap increases the potential for mixed infections and diversification.

While the eco-evolutionary framework developed here is grounded in the Mexican agroecosystem as its primary reference system, the comparative evidence presented below illustrates its broader global applicability. The concept of contact zones proposed here becomes especially relevant when examining parallels between Mexico and other regions where begomovirus emergence is associated with weed reservoirs, intercrops, and intensive agriculture. In Côte d’Ivoire, Yoboué et al. (36) conducted a nationwide survey of cassava agroecosystems and identified 65 plant species functioning as alternative hosts for cassava mosaic begomoviruses. Their study demonstrated that weeds and intercrops may sustain multiple begomoviruses and alphasatellites simultaneously, facilitating viral maintenance and spread between cultivated and non-cultivated systems. Similar to the Mexican agroecological interface, the West African system revealed that non-cultivated vegetation can act as a long-term viral reservoir connecting agricultural and natural environments.

Importantly, the African experience also illustrates how agroecosystem structure shapes surveillance needs. In cassava systems, begomovirus persistence is strongly linked to intercropping practices and the continuous availability of alternative hosts during off-season periods. This contrasts with Mexican pepper–tomato systems, where intensive horticultural production and overlapping viral communities appear to play a larger role in facilitating mixed infections and viral coexistence. Nevertheless, both systems highlight the importance of considering weeds and surrounding vegetation as integral components of begomovirus epidemiology rather than secondary ecological elements.

Comparative evidence from the Middle East further supports the need for integrated genomic surveillance. Recent HTS analyses in Saudi Arabia identified the co-circulation of TYLCV, watermelon chlorotic stunt virus (WmCSV, B. citrulli), and tomato leaf curl Palampur virus (ToLCPalV, B. solanumpalampurense) within cucurbit production systems, while also revealing the emergence of a novel TYLCV lineage (TYLCV-Hasa) (37). Population analyses suggested contrasting regional evolutionary dynamics, with some viral populations appearing genetically stable while others represented hotspots of admixture and diversification. These findings demonstrate that intensive agriculture, international trade, vector movement, and ecological overlap can collectively generate highly dynamic viral landscapes requiring continuous genomic monitoring.

From a management perspective, these observations support integrated surveillance frameworks that combine molecular diagnostics, HTS, vector ecology, weed management, resistant cultivars, and landscape-level epidemiological monitoring. Surveillance priorities may differ between endemic, invasive, and contact-zone systems depending on ecological connectivity, vector pressure, viral coexistence, and recombination potential (Table 1). Endemic systems may require reducing ecological continuity sustaining mixed infections and reservoir persistence, whereas introduced systems may require rapid detection and limitation of whitefly-mediated spread alongside monitoring of selection pressures generated by intensive production and resistance deployment (3, 12, 27, 28). Emerging sequencing technologies, including Oxford Nanopore approaches, may further strengthen surveillance capacity by enabling real-time characterization of mixed infections, recombinant variants, and invasive begomovirus population dynamics (41, 42).

Table 1. Eco-evolutionary surveillance framework for endemic and invasive begomovirus regimes.

ComponentEndemic regime: PHYVV/PepGMVInvasive regime: TYLCVIllustrative surveillance recommendationsKey references
Resident diversityMonitor PHYVV, PepGMV, and related begomoviruses in pepper agroecosystems.Assess whether TYLCV occurs where resident begomoviruses are present.Recommended approach: Genome sequencing. ≥20–30 symptomatic plants/region/crop cycle.ICTV ≥91% pairwise identity.21, 34, 38
Mixed infectionsPHYVV/PepGMV increase symptom severity and viral DNA.TYLCV detected with PHYVV/PepGMV.Suggested surveillance strategy:Multiplex PCR. Test all plants.Whole-genome sequencing if co-infection >10%.14, 15, 30
Recombination potentialDocumented in Mexican chiltepin-associated begomoviruses.Documented outside Mexico.Whole-genome sequencing + RDP5/SimPlot.Retain events supported by ≥3 methods (p<0.05).10, 18, 23, 31
Whitefly populationsThe whitefly transmits PHYVV/PepGMV.Transmission central to TYLCV.Operational recommendation: Biweekly sampling.mtCOI typing of ≥20–30 individuals/site.12, 13, 22
Non-cultivated hostsReservoir of diverse begomoviruses.Weeds may maintain TYLCV.Recommended sampling scheme: Survey field margins once/crop cycle.Prioritize Sida and Malvastrum.34, 39, 40
Agricultural contextCrop continuity supports circulation.Intensive production shapes selection.Document crop calendars, Ty-gene adoption and insecticide use.3, 27, 28
Contact zonesResident viral background.Overlap with resident begomoviruses.Sentinel plots.Monthly sampling across crop cycles.30, 34, 38

The suggested sampling efforts and thresholds listed under the surveillance-priority column are illustrative operational starting points intended to guide implementation and prioritization; they are not validated universal thresholds and should be calibrated to local epidemiological context.

To operationalize these recommendations, surveillance programs should incorporate the following specific actions: (i) sentinel plot sampling in pepper–tomato interface regions to monitor ecological overlap and early mixed-infection events; (ii) systematic collection of weeds and ruderal vegetation along agroecosystem edges, particularly in contact-zone areas; (iii) regular monitoring of whitefly populations with cryptic species identification using molecular markers to track biotype composition and invasive introductions; (iv) whole-genome sequencing of samples from mixed infections to detect recombination events and characterize novel viral variants; (v) temporal sampling across consecutive crop cycles to capture seasonal dynamics and multi-season evolutionary trends; (vi) application of recombination screening pipelines (e.g., RDP5, SimPlot) as standard components of begomovirus genomic surveillance; and (vii) integration of crop calendars, host plant distribution maps, and vector abundance data into spatially explicit epidemiological risk models for proactive surveillance planning. These values are proposed operational recommendations intended to illustrate surveillance implementation rather than validated universal thresholds.

Taken together, these findings support interpreting begomovirus emergence as an eco-evolutionary continuum rather than a collection of isolated epidemiological categories. In regions such as Mexico, West Africa, and the Middle East, where crop diversity, whitefly pressure, weed reservoirs, and intensive agriculture converge, surveillance frameworks integrating evolutionary biology, genomics, and agroecosystem ecology may help identify where viral persistence is likely to occur, where invasive lineages may become established, and where recombination-associated risks should be prioritized. Such an approach may ultimately shift begomovirus management from reactive outbreak response toward more anticipatory and risk-informed disease surveillance strategies.

4 Conclusion

Begomovirus emergence should be interpreted as an eco-evolutionary continuum shaped by interactions among viral diversity, whitefly transmission, alternative hosts, agricultural practices, and ecological connectivity. The comparison between endemic systems such as pepper huasteco yellow vein virus (PHYVV, B. capsicumhuastecoense) and pepper golden mosaic virus (PepGMV, B. capsicummusivi), and the invasive system represented by tomato yellow leaf curl virus (TYLCV, B. coheni), illustrates how resident and introduced viruses coexist within dynamic agroecosystems where mixed infections, recombination opportunities, and vector-mediated overlap may influence future epidemiological trajectories. Integrating genomic surveillance, high-throughput sequencing (HTS), vector ecology, and agroecosystem-level monitoring may improve early detection and support more proactive and risk-informed strategies for begomovirus disease management in Mexico and other vulnerable agricultural regions. More broadly, adopting an eco-evolutionary perspective shifts surveillance from reactive outbreak response toward anticipating the ecological conditions that favor viral emergence, diversification, and long-term persistence.

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Footnotes

Edited by: Nami Minato, Niigata University, Japan

Reviewed by: Massimiliano Morelli, National Research Council (CNR), Italy

Muhammad Zulqar Nain Dara, Jilin Agriculture University, China

Statements

Conflict of interest

The author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding

The author(s) declared that financial support was received for this work and/or its publication. FCAA received a postdoctoral fellowship from the Secretaría de Ciencia, Humanidades, Tecnología e Innovación (SECIHTI), CVU 229220.

Data availability

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

Author contributions

KA-P: Conceptualization, Formal analysis, Investigation, Writing – original draft, Writing – review & editing. FA-A: Conceptualization, Formal Analysis, Investigation, Writing – original draft, Writing – review & editing. EZ-M: Conceptualization, Formal analysis, Investigation, Writing – original draft, Writing – review & editing. UV: Conceptualization, Formal analysis, Investigation, Writing – original draft, Writing – review & editing. JC-T: Formal Analysis, Investigation, Writing – review & editing. AD-L: Conceptualization, Formal analysis, Investigation, Writing – original draft, Writing – review & editing.

Acknowledgements

The authors thank BioCódigo SAS for providing technical support, particularly Daniel Jacinto.

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Citation

Aviña-Padilla, K., et al. (2026). An eco-evolutionary perspective on endemic persistence and invasive emergence of begomoviruses in Mexico. Frontiers in Virology, Volume 6. https://doi.org/
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6 - 2026

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Copyright © 2026 Aviña-Padilla, Alcántar-Aguirre, Zamora-Macorra, Vasquez-Gutierrez, Carrillo-Tripp and Diaz-Lara.

License: https://creativecommons.org/licenses/by/4.0/

*Correspondence: Alfredo Diaz-Lara

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